Vol. 497: 157–178, 2014 MARINE ECOLOGY PROGRESS SERIES Published February 5 doi: 10.3354/meps10609 Mar Ecol Prog Ser Decadal diet shift in yellowfin tuna Thunnus albacares suggests broad-scale food web changes in the eastern tropical Pacific Ocean Robert J. Olson1,*, Leanne M. Duffy1, Petra M. Kuhnert2, Felipe Galván-Magaña3, Noemi Bocanegra-Castillo3,4, Vanessa Alatorre-Ramírez3 1Inter-American Tropical Tuna Commission, 8901 La Jolla Shores Drive, La Jolla, California 92037, USA 2CSIRO Computational Informatics, Private Bag 2, Glen Osmond, South Australia 5064, Australia 3Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, Apartado Postal 592, La Paz, Baja California Sur, CP 23000 México 4Present address: Centro de Investigaciones Biológicas del Noroeste SC, Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur, La Paz, Baja California Sur, CP 23096 México ABSTRACT: Widespread climate-induced habitat compression and reductions in biological pro- duction are beginning to alter food webs in tropical and subtropical oceans, but the effects on mid- trophic level micronekton communities that support commercially important pelagic fishes are unclear. The predation habits of yellowfin tuna Thunnus albacares, a wide-ranging generalist predator with high energy requirements, provide rare insights into the distribution and availabil- ity of prey communities in pelagic regions. We used a modified classification tree approach to ana- lyze spatial, temporal, environmental, and biological covariates explaining the predation patterns of 3362 yellowfin sampled across the eastern tropical Pacific Ocean (ETP) during two 2 yr periods occurring a decade apart. Persistent zoogeographical assemblages of prey were important only in relatively small subtropical regions at the extreme northern and southern ranges of the purse- seine fishery for tunas. Prey biomass patterns for the majority of the samples over most of the ETP (6° S to 17° N, coast to 150° W) were best explained by a tree partition distinguishing samples by sampling period, 1992 to 1994 and 2003 to 2005. The classification tree revealed that a major diet shift had transpired in the heart of the ETP. Yellowfin predation had changed from primarily larger epipelagic fish prey in the 1990s to a diverse array of smaller mesopelagic species and a crustacean that apparently had expanded its range in the 2000s. Partial dependence plots from the tree model showed range expansions previously described for some prey and unknown for other prey. Diet analysis of selected marine predators offers a practical means of monitoring prey communities poorly sampled by conventional methods. KEY WORDS: Classification and regression tree · Diet shift · Eastern Pacific · Food web · Predator−prey interaction · Trophic ecology · Tuna Resale or republication not permitted without written consent of the publisher INTRODUCTION flow in exploited ecosystems. Replacing population ecology with community ecology as the fundamental Increasing worldwide interest in ecologically based ecological science underlying fisheries (Mangel & approaches to fisheries management (Pikitch et al. Levin 2005) dictates a thorough understanding of the 2004, Marasco et al. 2007) places renewed emphasis dynamics of community interactions. ‘Food webs re- on understanding pathways of biomass and energy main the ecologically flexible scaffolding around *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 158 Mar Ecol Prog Ser 497: 157–178, 2014 which communities are assembled and structured’ Magaña 2002, Griffiths et al. 2009, Rabehagasoa (Paine 1996, p. ix). Determining linkages and measur- et al. 2012, Ménard et al. 2013). Unlike traditional ing interaction rates in the food web are prerequisites approaches for analyzing diet data, classification for gaining insight into the role of predators, commer- trees provide a modeling framework for predicting cial fisheries, and the environment in influencing eco- the prey composition of each predator and can high- system structure and dynamics (Watters et al. 2003). light important relationships between explanatory Marine ecologists are challenged by questions about variables and the response (Breiman et al. 1984, the implications of climate- and fisheries-induced Clarke & Pregibon 1992). ecosystem changes. Environmental perturbations Our approach was to examine broad-scale spatial, force ecosystems from the bottom up, while selective temporal, environmental, and biological relationships removal of large predatory fishes from marine food with predator−prey data for yellowfin tuna in the ETP webs can simultaneously impart top-down changes using a modified classification tree approach devel- in trophic structure and stability via trophic cascades oped for diet data by Kuhnert et al. (2012). Our ob - (Carpenter et al. 1985, Pace et al. 1999, McClanahan jectives were to (1) elucidate the dominant predator− & Arthur 2001, Worm & Myers 2003, Essington & prey patterns characterizing the trophic ecology of Hansson 2004, Frank et al. 2005). Major reorganiza- the yellowfin population in the ETP, and (2) examine tions of food webs have occurred in concert with the degree and scale of diet variability on a decadal environmental changes in large marine ecosystems, time frame. This analysis is an essential component notably in the Northeast Pacific Ocean (Anderson & for developing improved food web models (e.g. Cox Piatt 1999, Conners et al. 2002) during shifts in the et al. 2002, Olson & Watters 2003) for examining Pacific Decadal Oscillation (PDO) (Hare & Mantua hypotheses of ecosystem effects of fishing over a 2000). The mechanisms linking climate forcing to backdrop of climate variation (Watters et al. 2003). changes in food webs are not clear (Johnson & Schindler 2012), and thus comparative and observa- tional approaches using historical data are required MATERIALS AND METHODS (Francis & Hare 1994). Changes through time in the structure of pelagic, Stomach sampling and analysis open-ocean food webs are difficult to assess. Fish- eries-independent trawl surveys are expensive and Yellowfin were captured in 433 purse-seine sets on pelagic trawls are often biased against larger, active dolphins, floating objects, and unassociated schools in micronekton (Young et al. 2001, Bertrand et al. 2002, the ETP during two 2-year periods separated by a Ménard et al. 2006). The foraging patterns of tropical decade. In ‘dolphin sets’ the net is deployed around a tunas, however, can provide useful information on tuna−dolphin aggregation (Scott et al. 2012) after a mid-trophic level communities in pelagic habitats chase by speedboats, ‘floating-object sets’ are made (Lansdell & Young 2007). The yellowfin tuna Thunnus by encircling flotsam (commonly fish-aggregating de- albacares is considered an opportunistic predator vices) and associated fauna with the purse seine, and (Sund et al. 1981, Ménard et al. 2006, Potier et al. ‘unassociated sets’ are made on schools of tuna that 2007, Young et al. 2010), owing to a generalized feed- are not associated with either mammals or flotsam ing strategy and high energy requirements in oligo- (Hall 1998). Dolphin sets and unassociated sets were trophic habitats. It is abundant, wide ranging, and an made fairly uniformly throughout the day, while most important component of the pelagic ecosystem in the floating-object sets were made in the early morning. eastern tropical Pacific Ocean (ETP) (Olson & Watters The sampling locations (Fig. 1) were distributed 2003), as it is in all the major oceans. Annual catches throughout the region in which yellowfin tuna were of yellowfin in the eastern Pacific averaged in excess caught by purse seine during both sampling periods of 290 000 metric tons, 91% by purse seine, during the (see Fig. A-1a in IATTC 2006 for catch locations). years of this study (IATTC 2012). Stomachs were collected at sea by Inter-American Classification and regression tree (CART) analysis, Tropical Tuna Commission (IATTC) ob servers on 212 a non-parametric approach developed by Breiman et purse-seine fishing trips between June 23, 1992 and al. (1984), has provided insight into the interpretation September 29, 1994, and between August 11, 2003 of a variety of complex ecological data (e.g. Olden & and November 16, 2005. Observers recorded the date, Jackson 2002, Zuur et al. 2007, Massey et al. 2008, time, location, fishing method, cloud cover, Beaufort Davidson et al. 2009), including foraging ecology sea state, and sea surface temperature (SST) for each (Iverson et al. 1997, Smith et al. 1997, Olson & Galván- set sampled. They measured fork length to the nearest Olson et al.: Diet shift in yellowfin tuna 159 were divided by 2 to estimate numbers of individual organisms ingested. Diet composition We used gravimetric, numeric, and occurrence in dices to examine prey importance. For each individual yel- lowfin, we calculated the proportional composition by weight and by number of each prey type, and then averaged the proportions for each prey type over all yellowfin with prey remains in the stomachs (Chipps & Garvey 2007). For prey weights: ⎛ ⎞ Wij 1 P ⎜ ⎟ W = ⎜ Q ⎟ (1) i P ∑ j=1⎜ ∑Wij ⎟ Fig. 1. Sampling locations of yellowfin tuna caught by purse-seine vessels dur- ⎝⎜ i=1 ⎠⎟ ing two 2-year periods in the eastern tropical Pacific Ocean. Sample sizes for all stomachs (open triangles) and for stomachs containing undigested prey re- where W- is mean proportion by mains (i.e. omitting samples that were empty or contained